Moving beyond linear food chains: trait-mediated indirect interactions in a rocky intertidal food web

In simple, linear food chains, top predators can have positive indirect effects on basal resources by causing changes in the traits (e.g. behaviour, feeding rates) of intermediate consumers. Although less is known about trait-mediated indirect interactions (TMIIs) in more complex food webs, it has been suggested that such complexity dampens trophic cascades. We examined TMIIs between a predatory crab (Carcinus maenas) and two ecologically important basal resources, fucoid algae (Ascophyllum nodosum) and barnacles (Semibalanus balanoides), which are consumed by herbivorous (Littorina littorea) and carnivorous (Nucella lapillus) snails, respectively. Because crab predation risk suppresses snail feeding rates, we hypothesized that crabs would also shape direct and indirect interactions among the multiple consumers and resources. We found that the magnitude of TMIIs between the crab and each resource depended on the suite of intermediate consumers present in the food web. Carnivorous snails (Nucella) transmitted TMIIs between crabs and barnacles. However, crab–algae TMIIs were transmitted by both herbivorous (Littorina) and carnivorous (Nucella) snails, and these TMIIs were additive. By causing Nucella to consume fewer barnacles, crab predation risk allowed fucoids that had settled on or between barnacles to remain in the community. Hence, positive interactions between barnacles and algae caused crab–algae TMIIs to be strongest when both consumers were present. Studies of TMIIs in more realistic, reticulate food webs will be necessary for a more complete understanding of how predation risk shapes community dynamics.

在简单的线性食物链中，顶级捕食者可通过改变中间消费者的性状（如行为、摄食速率），对基础资源产生正向间接效应。尽管目前针对复杂食物网中的性状介导的间接相互作用（trait-mediated indirect interactions, TMIIs）的研究尚少，但已有研究指出，食物网的复杂性会削弱营养级联效应。本研究针对捕食性蟹（普通滨蟹*Carcinus maenas*）与两类具有重要生态意义的基础资源——褐藻（墨角藻*Ascophyllum nodosum*）和藤壶（白纹藤壶*Semibalanus balanoides*）之间的性状介导间接相互作用展开探究，其中褐藻与藤壶分别为草食性滨螺（*Littorina littorea*）与肉食性峨螺（*Nucella lapillus*）的摄食对象。由于蟹的捕食风险会抑制螺类的摄食速率，我们提出假说：蟹同样会调控多种消费者与基础资源之间的直接与间接相互作用。研究结果显示，蟹与各基础资源之间的性状介导间接相互作用强度，取决于食物网中存在的中间消费者类群组合。肉食性峨螺（*Nucella*）可介导蟹与藤壶之间的性状介导间接相互作用；但蟹与褐藻之间的性状介导间接相互作用，可同时由草食性滨螺（*Littorina*）与肉食性峨螺（*Nucella*）介导，且二者的效应具有加和性。蟹的捕食风险会降低峨螺的藤壶摄食量，使得附着于藤壶表面或藤壶间隙的褐藻得以留存于群落中。因此，当两类中间消费者同时存在时，藤壶与褐藻之间的正向相互作用会使蟹与褐藻之间的性状介导间接相互作用强度达到峰值。若要全面理解捕食风险如何塑造群落动态，有必要在更贴近自然的网状食物网中开展性状介导间接相互作用相关研究。